Regulation of hetDNA Length during Mitotic Double-Strand Break Repair in Yeast

Molecular Cell

Volumn 67, Issue 4, 2017, Pages 539-549.e4

  Guo, Xiaoge ^a,b   Hum, Yee Fang ^a   Lehner, Kevin ^a,c   Jinks Robertson, Sue ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

crossover; DNA polymerase; double strand break repair; gene conversion; heteroduplex DNA; recombination; resection

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I; FUNGAL DNA; HETERODUPLEX; RECQ HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN; SGS1 PROTEIN, S CEREVISIAE;

DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM;

DNA BREAKS, DOUBLE-STRANDED; DNA POLYMERASE III; DNA REPAIR; DNA, FUNGAL; EXODEOXYRIBONUCLEASES; GENOTYPE; MITOSIS; MUTATION; NUCLEIC ACID HETERODUPLEXES; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 85027543495     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.07.009     Document Type: Article

References (87)

1. Aguilera, A., Klein, H.L., Yeast intrachromosomal recombination: long gene conversion tracts are preferentially associated with reciprocal exchange and require the RAD1 and RAD3 gene products. Genetics 123 (1989), 683–694.
2. Ahn, B.-Y., Livingston, D.M., Mitotic gene conversion lengths, coconversion patterns, and the incidence of reciprocal recombination in a Saccharomyces cerevisiae plasmid system. Mol. Cell. Biol. 6 (1986), 3685–3693.
3. Anand, R., Beach, A., Li, K., Haber, J., Rad51-mediated double-strand break repair and mismatch correction of divergent substrates. Nature 544 (2017), 377–380.
4. Andres, S.N., Appel, C.D., Westmoreland, J.W., Williams, J.S., Nguyen, Y., Robertson, P.D., Resnick, M.A., Williams, R.S., Tetrameric Ctp1 coordinates DNA binding and DNA bridging in DNA double-strand-break repair. Nat. Struct. Mol. Biol. 22 (2015), 158–166.
5. Burgers, P.M., Gerik, K.J., Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase δ. J. Biol. Chem. 273 (1998), 19756–19762.
6. Cejka, P., DNA end resection: nucleases team up with the right partners to initiate homologous recombination. J. Biol. Chem. 290 (2015), 22931–22938.
7. Cejka, P., Cannavo, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J.L., Kowalczykowski, S.C., DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467 (2010), 112–116.
8. Chen, X., Niu, H., Chung, W.H., Zhu, Z., Papusha, A., Shim, E.Y., Lee, S.E., Sung, P., Ira, G., Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat. Struct. Mol. Biol. 18 (2011), 1015–1019.
9. Chen, X., Cui, D., Papusha, A., Zhang, X., Chu, C.D., Tang, J., Chen, K., Pan, X., Ira, G., The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489 (2012), 576–580.
10. Chu, W.K., Hickson, I.D., RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer 9 (2009), 644–654.
11. Chua, P., Jinks-Robertson, S., Segregation of recombinant chromatids following mitotic crossing over in yeast. Genetics 129 (1991), 359–369.
12. Chung, W.H., Zhu, Z., Papusha, A., Malkova, A., Ira, G., Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet., 6, 2010, e1000948.
13. de Massy, B., Rocco, V., Nicolas, A., The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J. 14 (1995), 4589–4598.
14. De Muyt, A., Jessop, L., Kolar, E., Sourirajan, A., Chen, J., Dayani, Y., Lichten, M., BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol. Cell 46 (2012), 43–53.
15. Eapen, V.V., Sugawara, N., Tsabar, M., Wu, W.H., Haber, J.E., The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol. Cell. Biol. 32 (2012), 4727–4740.
16. Ferrari, M., Dibitetto, D., De Gregorio, G., Eapen, V.V., Rawal, C.C., Lazzaro, F., Tsabar, M., Marini, F., Haber, J.E., Pellicioli, A., Functional interplay between the 53BP1-ortholog Rad9 and the Mre11 complex regulates resection, end-tethering and repair of a double-strand break. PLoS Genet., 11, 2015, e1004928.
17. Fleig, U.N., Pridmore, R.D., Philippsen, P., Construction of LYS2 cartridges for use in genetic manipulations of Saccharomyces cerevisiae. Gene 46 (1986), 237–245.
18. Giot, L., Chanet, R., Simon, M., Facca, C., Faye, G., Involvement of the yeast DNA polymerase delta in DNA repair in vivo. Genetics 146 (1997), 1239–1251.
19. Goldstein, A.L., McCusker, J.H., Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15 (1999), 1541–1553.
20. Gravel, S., Chapman, J.R., Magill, C., Jackson, S.P., DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22 (2008), 2767–2772.
21. Gueldener, U., Heinisch, J., Koehler, G.J., Voss, D., Hegemann, J.H., A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res., 30, 2002, e23.
22. Güldener, U., Heck, S., Fielder, T., Beinhauer, J., Hegemann, J.H., A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24 (1996), 2519–2524.
23. Guo, X., Jinks-Robertson, S., Roles of exonucleases and translesion synthesis DNA polymerases during mitotic gap repair in yeast. DNA Repair (Amst.) 12 (2013), 1024–1030.
24. Guo, X., Lehner, K., O'Connell, K., Zhang, J., Dave, S.S., Jinks-Robertson, S., SMRT sequencing for parallel analysis of multiple targets and accurate SNP phasing. G3 (Bethesda) 5 (2015), 2801–2808.
25. Ho, C.K., Mazón, G., Lam, A.F., Symington, L.S., Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol. Cell 40 (2010), 988–1000.
26. Hopfner, K.P., Craig, L., Moncalian, G., Zinkel, R.A., Usui, T., Owen, B.A., Karcher, A., Henderson, B., Bodmer, J.L., McMurray, C.T., et al. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418 (2002), 562–566.
27. Inbar, O., Kupiec, M., Homology search and choice of homologous partner during mitotic recombination. Mol. Cell. Biol. 19 (1999), 4134–4142.
28. Inbar, O., Liefshitz, B., Bitan, G., Kupiec, M., The relationship between homology length and crossing over during the repair of a broken chromosome. J. Biol. Chem. 275 (2000), 30833–30838.
29. Ira, G., Malkova, A., Liberi, G., Foiani, M., Haber, J.E., Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003), 401–411.
30. Jain, S., Sugawara, N., Lydeard, J., Vaze, M., Tanguy Le Gac, N., Haber, J.E., A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev. 23 (2009), 291–303.
31. Jin, Y.H., Obert, R., Burgers, P.M., Kunkel, T.A., Resnick, M.A., Gordenin, D.A., The 3′–>5′ exonuclease of DNA polymerase δ can substitute for the 5′ flap endonuclease Rad27/Fen1 in processing Okazaki fragments and preventing genome instability. Proc. Natl. Acad. Sci. USA 98 (2001), 5122–5127.
32. Jinks-Robertson, S., Petes, T.D., Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics 114 (1986), 731–752.
33. Jinks-Robertson, S., Michelitch, M., Ramcharan, S., Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 13 (1993), 3937–3950.
34. Johnson, S.J., Beese, L.S., Structures of mismatch replication errors observed in a DNA polymerase. Cell 116 (2004), 803–816.
35. Johnson, R.E., Prakash, L., Prakash, S., Pol31 and Pol32 subunits of yeast DNA polymerase δ are also essential subunits of DNA polymerase ζ. Proc. Natl. Acad. Sci. USA 109 (2012), 12455–12460.
36. Kunkel, T.A., Exonucleolytic proofreading. Cell 53 (1988), 837–840.
37. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
38. Lazzaro, F., Sapountzi, V., Granata, M., Pellicioli, A., Vaze, M., Haber, J.E., Plevani, P., Lydall, D., Muzi-Falconi, M., Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 27 (2008), 1502–1512.
39. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
40. Li, X., Stith, C.M., Burgers, P.M., Heyer, W.D., PCNA is required for initiation of recombination-associated DNA synthesis by DNA polymerase δ. Mol. Cell 36 (2009), 704–713.
41. Liu, J., Wu, T.C., Lichten, M., The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J. 14 (1995), 4599–4608.
42. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T)) Method. Methods 25 (2001), 402–408.
43. Llorente, B., Symington, L.S., The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol. Cell. Biol. 24 (2004), 9682–9694.
44. Longtine, M.S., McKenzie, A. 3rd, Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P., Pringle, J.R., Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998), 953–961.
45. Lyndaker, A.M., Alani, E., A tale of tails: insights into the coordination of 3′ end processing during homologous recombination. BioEssays 31 (2009), 315–321.
46. Maloisel, L., Bhargava, J., Roeder, G.S., A role for DNA polymerase delta in gene conversion and crossing over during meiosis in Saccharomyces cerevisiae. Genetics 167 (2004), 1133–1142.
47. Maloisel, L., Fabre, F., Gangloff, S., DNA polymerase δ is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Mol. Cell. Biol. 28 (2008), 1373–1382.
48. Marrero, V.A., Symington, L.S., Extensive DNA end processing by exo1 and sgs1 inhibits break-induced replication. PLoS Genet., 6, 2010, e1001007.
49. Mazón, G., Symington, L.S., Mph1 and Mus81-Mms4 prevent aberrant processing of mitotic recombination intermediates. Mol. Cell 52 (2013), 63–74.
50. McCulloch, S.D., Kokoska, R.J., Chilkova, O., Welch, C.M., Johansson, E., Burgers, P.M., Kunkel, T.A., Enzymatic switching for efficient and accurate translesion DNA replication. Nucleic Acids Res. 32 (2004), 4665–4675.
51. McVey, M., Khodaverdian, V.Y., Meyer, D., Cerqueira, P.G., Heyer, W.D., Eukaryotic DNA polymerases in homologous recombination. Annu. Rev. Genet. 50 (2016), 393–421.
52. Miller, H., Grollman, A.P., Kinetics of DNA polymerase I (Klenow fragment exo-) activity on damaged DNA templates: effect of proximal and distal template damage on DNA synthesis. Biochemistry 36 (1997), 15336–15342.
53. Mimitou, E.P., Symington, L.S., Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455 (2008), 770–774.
54. Mimitou, E.P., Symington, L.S., Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J. 29 (2010), 3358–3369.
55. Mitchel, K., Zhang, H., Welz-Voegele, C., Jinks-Robertson, S., Molecular structures of crossover and noncrossover intermediates during gap repair in yeast: implications for recombination. Mol. Cell 38 (2010), 211–222.
56. Mitchel, K., Lehner, K., Jinks-Robertson, S., Heteroduplex DNA position defines the roles of the Sgs1, Srs2, and Mph1 helicases in promoting distinct recombination outcomes. PLoS Genet., 9, 2013, e1003340.
57. Miura, T., Yamana, Y., Usui, T., Ogawa, H.I., Yamamoto, M.T., Kusano, K., Homologous recombination via synthesis-dependent strand annealing in yeast requires the Irc20 and Srs2 DNA helicases. Genetics 191 (2012), 65–78.
58. Moreau, S., Ferguson, J.R., Symington, L.S., The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19 (1999), 556–566.
59. Morrison, A., Sugino, A., The 3′–>5′ exonucleases of both DNA polymerases δ and ε participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol. Gen. Genet. 242 (1994), 289–296.
60. Morrison, A., Bell, J.B., Kunkel, T.A., Sugino, A., Eukaryotic DNA polymerase amino acid sequence required for 3′—-5′ exonuclease activity. Proc. Natl. Acad. Sci. USA 88 (1991), 9473–9477.
61. Niu, H., Chung, W.H., Zhu, Z., Kwon, Y., Zhao, W., Chi, P., Prakash, R., Seong, C., Liu, D., Lu, L., et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467 (2010), 108–111.
62. Pâques, F., Haber, J.E., Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 17 (1997), 6765–6771.
63. Pâques, F., Leung, W.Y., Haber, J.E., Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol. Cell. Biol. 18 (1998), 2045–2054.
64. Paull, T.T., Gellert, M., The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998), 969–979.
65. Prolla, T.A., Christie, D.-M., Liskay, R.M., Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutL gene. Mol. Cell. Biol. 14 (1994), 407–415.
66. Rattray, A.J., Shafer, B.K., McGill, C.B., Strathern, J.N., The roles of REV3 and RAD57 in double-strand-break-repair-induced mutagenesis of Saccharomyces cerevisiae. Genetics 162 (2002), 1063–1077.
67. Roberts, S.A., Sterling, J., Thompson, C., Harris, S., Mav, D., Shah, R., Klimczak, L.J., Kryukov, G.V., Malc, E., Mieczkowski, P.A., et al. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46 (2012), 424–435.
68. Roy, R., Chun, J., Powell, S.N., BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat. Rev. Cancer 12 (2011), 68–78.
69. Saad, H., Gallardo, F., Dalvai, M., Tanguy-le-Gac, N., Lane, D., Bystricky, K., DNA dynamics during early double-strand break processing revealed by non-intrusive imaging of living cells. PLoS Genet., 10, 2014, e1004187.
70. Shcherbakov, V.P., Plugina, L.A., Kudryashova, E.A., Marker-dependent recombination in T4 bacteriophage. IV. Recombinational effects of antimutator T4 DNA polymerase. Genetics 140 (1995), 13–25.
71. Shim, E.Y., Chung, W.H., Nicolette, M.L., Zhang, Y., Davis, M., Zhu, Z., Paull, T.T., Ira, G., Lee, S.E., Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J. 29 (2010), 3370–3380.
72. Sikorski, R.S., Hieter, P., A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122 (1989), 19–27.
73. Stone, J.E., Petes, T.D., Analysis of the proteins involved in the in vivo repair of base-base mismatches and four-base loops formed during meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 173 (2006), 1223–1239.
74. Storici, F., Durham, C.L., Gordenin, D.A., Resnick, M.A., Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc. Natl. Acad. Sci. USA 100 (2003), 14994–14999.
75. Stracker, T.H., Petrini, J.H., The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol. 12 (2011), 90–103.
76. Symington, L.S., Mechanism and regulation of DNA end resection in eukaryotes. Crit. Rev. Biochem. Mol. Biol. 51 (2016), 195–212.
77. Symington, L.S., Kang, L.E., Moreau, S., Alteration of gene conversion tract length and associated crossing over during plasmid gap repair in nuclease-deficient strains of Saccharomyces cerevisiae. Nucleic Acids Res. 28 (2000), 4649–4656.
78. Symington, L.S., Rothstein, R., Lisby, M., Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198 (2014), 795–835.
79. Thomas, B.J., Rothstein, R., The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene. Genetics 123 (1989), 725–738.
80. Travers, K.J., Chin, C.S., Rank, D.R., Eid, J.S., Turner, S.W., A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res., 38, 2010, e159.
81. Welz-Voegele, C., Jinks-Robertson, S., Sequence divergence impedes crossover more than noncrossover events during mitotic gap repair in yeast. Genetics 179 (2008), 1251–1262.
82. Westmoreland, J.W., Resnick, M.A., Coincident resection at both ends of random, γ-induced double-strand breaks requires MRX (MRN), Sae2 (Ctp1), and Mre11-nuclease. PLoS Genet., 9, 2013, e1003420.
83. Wu, L., Hickson, I.D., The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426 (2003), 870–874.
84. Yim, E., O'Connell, K.E., St Charles, J., Petes, T.D., High-resolution mapping of two types of spontaneous mitotic gene conversion events in Saccharomyces cerevisiae. Genetics 198 (2014), 181–192.
85. Zakharyevich, K., Tang, S., Ma, Y., Hunter, N., Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149 (2012), 334–347.
86. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E., Ira, G., Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134 (2008), 981–994.
87. Zierhut, C., Diffley, J.F., Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27 (2008), 1875–1885.